Low-frequency brain oscillations reflect the dynamics of the oculomotor system: a new perspective on subsequent memory effects

Abstract

Neural activity and eye movements are two well-established predictors of memory performance in humans. Successful memory formation is typically associated with reduced alpha/beta power (i.e., the alpha/beta subsequent memory effect) and an increased number of eye movements. However, the functional relevance of these two memory correlates has primarily been investigated in isolation, leaving their coupling and combined contribution to memory formation largely unknown. Here, we address this gap through four experiments involving simultaneous eye-tracking and scalp or intracranial electroencephalography recordings while participants viewed scenes either freely or under varying levels of visual constraint. Across experiments and cohorts, we identified the degree of visual exploration, rather than subsequent memory performance, as the consistent and robust modulator of alpha/beta power reductions. Going beyond correlations, manipulating eye movements dissociated alpha/beta power reductions from memory. Combined with the finding that saccade parameters predicted the dynamics of alpha/beta activity, our results directly link alpha/beta activity to the oculomotor system. Moreover, we show that the accumulation of saccades over time accounted for the reduced alpha/beta power, resembling the pattern typically observed after stimulus onset. Our work demonstrates that neglecting eye movements results in an incomplete understanding of the alpha/beta subsequent memory effect. Together, the evidence points at alpha/beta activity directly reflecting eye movements, and only indirectly, memory formation. The current study thus bridges two lines of previous research and advocates for new perspectives on the specific interpretation of the alpha/beta subsequent memory effect and on the function of alpha/beta activity in general.